Social Transmission Of Food Preferences Research Articles

Evaluating and re-evaluating intra- and inter-species social transmission of food preferences in domestic dogs

Social-transmission of food preference is a robust behavioral phenomenon in rodents and other species, but less work has evaluated this phenomenon in broader taxa and to what degree social-transmission can occur between species. Here we show that over the span of three experiments that consisted of a human-dog, a dog-dog, and a replication study of a dog-dog demonstrator-observer test, we did not observe successful social transmission of food preferences across all three experiments. For our first experiment, we investigated whether pet dogs acquire food preference from their owners using a two-bowl preference test. The results suggested that our dogs did not acquire a preference for the flavor consumed by their owners. This then led us to investigate whether this failure was the result of an inter-species failure, so we replicated the experiment using two familiar dogs as the demonstrator and observer. The results for Experiment Two also suggested that our participant dogs do not acquire food preference from a canine demonstrator. A third experiment attempted a direct replication of the Lupfer-Johnson and Ross (2007) that found dog-dog transmission of food preferences. Our results again indicated that our participant dogs did not acquire food preference from demonstrators. Over the span of three experiments, our results did not show clear canine food preferences for the food consumed by a demonstrator (human or dog).

Does demonstrator relevance affect social preferences and the social transmission of food preferences in female mice (Mus musculus)?

This study examined whether a history of beneficial social learning experiences affects social partner preferences in laboratory mice (Mus musculus) and whether observer mice acquire adaptive model-based social learning strategies through associative learning. We tested whether observers would come to socially prefer demonstrators who provide beneficial information through the social transmission of food preference (STFP), over demonstrators who do not; and whether they would preferentially attend to and learn from such demonstrators. Observers were given repeated exposures to two demonstrators who differed in whether or not they consistently provided beneficial information (which increased observers’ ingestion of food via the STFP). After multiple social learning experiences with a “relevant demonstrator” (our CS+) whose demonstrated food was available for consumption (our US) by the observer and a “non-relevant demonstrator” whose demonstrated food was never encountered, neither demonstrator was preferred over the other. Furthermore, observers learned equally well from both relevant and non-relevant demonstrators. The present findings suggest that adaptive model-based social learning strategies are not followed in the STFP, although we recommend further testing of the social preference hypothesis.

Differing effects of familiarity/kinship in the social transmission of fear associations and food preferences in rats.

Despite its apparent adaptive advantages, past research has found that greater familiarity and/or familial relatedness of a social demonstrator does not enhance social learning in the social transmission of food preference paradigm. This finding runs counter to research examining the effects of demonstrator characteristics in fear-mediated social learning paradigms, in which increased familiarity and/or relatedness of a demonstrator promotes higher rates of learning in observer rats. In our first experiment, we were able to corroborate the finding that increased familiarity/relatedness to the demonstrator does not enhance acquisition of a socially transmitted food preference. Furthermore, on examination of the social behavior between observers and their demonstrators during the acquisition of a socially transmitted food preference, no analogous relationship between social contact and expression of the learned preference was observed. In our second experiment, we provide further evidence that familiarity/relatedness may enhance the social acquisition of a fear response to an otherwise neutral auditory cue and demonstrate that this effect is not solely the result of increased social contact between the observer and their demonstrator during acquisition. Despite similar levels of post-cue contact in both observer types, a positive correlation was observed between post-cue social contact and expression of a socially acquired fear behavior when the observer was familiar/related to their demonstrator but not novel/unrelated. These findings both validate previous research on the role of familiarity/relatedness in these two social learning paradigms and provide further behavioral evidence that unique social mechanisms may serve to mediate the social transmission of fear.

Assessment of Social Transmission of Food Preferences Behaviors.

Olfactory recognition deficits are suggested to be able to serve as clinical marker to differentiate Alzheimer's disease (AD) subjects from healthy aging groups. For example, olfactory dysfunction in AD can present as impairment in olfactory recognition, emerging during early stages of the disease and worsening while the disease progresses. The social transmission of food preferences (STFP) task is based on a rudimentary form of communication between rodents concerning distant foods dependent on the transmission of olfactory cues. Healthy wild-type mice would prefer to eat a novel, flavored food that was previously cued by a conspecific, and this food preference would be hampered in transgenic AD mice, such as the APP/PS1 model. Indeed, a strong preference for the cued food in C57Bl6/J mice of 3 months of age was found, and this was reduced in 3 months old transgenic APP/PS1 mice. In summary, STFP task could be a powerful measure to be integrated in present subclinical detection assays of AD.

Effects of scopolamine on social transmission of food preferences

Rats must forage adaptively, choose safe foods, and avoid poisonous foods. The social transmission of food preference paradigm is useful to study learning and memory. Several studies have found that the associations formed in that paradigms are examples of declarative memory. Scopolamine induces interference in learning and consolidation of memories in diverse tasks. In this experiment, we evaluated the effect of one dose of the drug on the memory formed in several trials of this paradigm. In three groups, we evaluated the effect of administering saline and scopolamine with a control group that received no treatment. Results showed that the dose of scopolamine interfered with the consolidation of a series of trials in the transmission of preference. We discussed the effect in relation to different studies that used different tasks. The results support that scopolamine impaired consolidation on social transmission of food preference.

The Role of Dorsal Hippocampal Dopamine D1-Type Receptors in Social Learning, Social Interactions, and Food Intake in Male and Female Mice.

The neurobiological mechanisms underlying social learning (ie, in which an animal's learning is influenced by another) are slowly being unraveled. Previous work with systemic treatments shows that dopamine (DA) D1-type receptors mediate social learning in the social transmission of food preferences (STFP) in mice. This study examines the involvement of one brain region underlying this effect. The ventral tegmental area has dopaminergic projections to many limbic structures, including the hippocampus-a site important for social learning in the STFP in rodents. In this study, adult male and female CD-1 mice received a dorsal hippocampal microinfusion of the D1-like receptor antagonist SCH23390 at 1, 2, 4, or 6 μg/μl 15 min before a 30 min social interaction with a same-sex conspecific, in which mice had the opportunity to learn a socially transmitted food preference. Results show that social learning was blocked in female mice microinfused with 6 μg/μl, and in males infused with 1, 4, or 6 μg/μl of SCH23390. This social learning impairment could not be explained by changes in total food intake, or olfactory discrimination. A detailed analysis of the social interactions also revealed that although SCH23390 did not affect oronasal investigation for either sex, drug treatments affected other social behaviors in a sex-specific manner; there was primarily a reduction in agonistic-related behaviors among males, and social investigatory-related behaviors among females. Thus, this study shows that dorsal hippocampal D1-type receptors mediate social learning and social behaviors in male and female mice.

Stereotypic mice are aggressed by their cage-mates, and tend to be poor demonstrators in social learning tasks

AbstractStereotypic behaviours (SBs) are linked with behavioural inflexibility and resemble symptoms of autism, suggesting that stereotypic animals could have autistic-like social impairments. SBs are also common in caged mice. We therefore hypothesised relationships between stereotypic and social behaviours, predicting that highly stereotypic mice would give/receive more agonism and be less effective in social learning tasks. Experiment One used C57BL/6 and DBA/2 mice in non-enriched or enriched housing (15 cages each); Experiment Two, more cages (six non-enriched, 44 enriched) plus a third strain (BALB/c). Across both experiments, enrichment reduced SB and agonism (aggression, plus ‘displacements’ where one mouse supplants another at a resource). These effects appeared related: housing effects on agonism became negligible when SB was statistically controlled for, and, at least in enriched cages, SB covaried with receiving aggression. In Experiment Three, 20 DBAs varying in SB from Experiment Two acted as demonstrators in a ‘social transmission of food preferences’ task. They were fed a novel flavour (shatavari powder), then each mingled with a familiar but flavour-naïve C57 observer. Observers were subsequently offered two novel flavours: shatavari or marjoram. Those spontaneously choosing more shatavari (n = 10) tended to have had less stereotypic demonstrators than the other ten observer mice. Overall, highly stereotypic mice thus received more agonism — an effect with obvious welfare implications that can be reduced with enrichment — and seemed potentially less effective at inducing flavour preferences in conspecifics. Such effects are consistent with social impairment, suggesting that reducing SB may perhaps enhance interactions between conspecifics.

Activation of the G protein-coupled estrogen receptor, but not estrogen receptor α or β, rapidly enhances social learning

Social learning is a highly adaptive process by which an animal acquires information from a conspecific. While estrogens are known to modulate learning and memory, much of this research focuses on individual learning. Estrogens have been shown to enhance social learning on a long-term time scale, likely via genomic mechanisms. Estrogens have also been shown to affect individual learning on a rapid time scale through cell-signaling cascades, rather than via genomic effects, suggesting they may also rapidly influence social learning. We therefore investigated the effects of 17β-estradiol and involvement of the estrogen receptors (ERs) using the ERα agonist propyl pyrazole triol, the ERβ agonist diarylpropionitrile, and the G protein-coupled ER 1 (GPER1) agonist G1 on the social transmission of food preferences (STFP) task, within a time scale that focused on the rapid effects of estrogens. General ER activation with 17β-estradiol resulted in a modest facilitation of social learning, with mice showing a preference up to 30min of testing. Specific activation of the GPER1 also rapidly enhanced social learning, with mice showing a socially learned preference up to 2h of testing. ERα activation instead shortened the expression of a socially learned food preference, while ERβ activation had little to no effects. Thus, rapid estrogenic modulation of social learning in the STFP may be the outcome of competing action at the three main receptors. Hence, estrogens' rapid effects on social learning likely depend on the specific ERs present in brain regions recruited during social learning.

Avoidance of potentially harmful food cannot be socially transmitted between rats.

The social transmission of food preferences (STFP) is a behavioural task of olfactory memory, in which an observer rat learns safe food odours from a demonstrator rat, and shows preference for this odour in a subsequent choice test. However, previous studies have failed to detect the transmission of information about food of potential danger and food aversion using STFP test. In this study, we tested how demonstrators' health affects the exchange of odour information and whether observers can learn danger information from an unhealthy demonstrator. As expected, the observer rat formed an odour preference after interacting with a demonstrator rat that had just eaten food containing a new odour, however, odour preference rather than aversion was also formed after interacting with a demonstrator rat injected with LiCl (used to induce gastric malaise). Furthermore, anaesthetized demonstrator rats and half-anaesthetized demonstrator rats, which showed obvious motor deficits suggesting an unhealthy state, also socially transmitted food preferences to observers. These results suggest that the social transmission of food preferences task is independent of a demonstrators' health, and that information about dangerous foods cannot be transmitted using this behavioural task.

Effect of Nutrient Restriction on Social Transmission of Food Preferences Depends on Nutrient and Species

For omnivores to determine whether an unfamiliar item is an appropriate food, they could rely on personal information from sampling it themselves or rely on less risky observation of whether other individuals eat the item. Availability of information about food from social companions in group-living species is one of the benefits of group life. Adults of solitary-living species, however, seem typically less likely to rely on social information about food choice. If an individual faced a nutritional deficit, it would seem to increase the value of public information. This study addresses whether dietary restriction from certain nutrients (sodium, potassium, protein, carbohydrates) affects reliance on information about food from conspecifics. Without nutrient restriction, group-living Norway rats (Rattus norvegicus) preferred the diet that they smelled on the breath of a conspecific demonstrator, but solitary-living Syrian hamsters (Mesocricetus auratus) avoided it. Protein restriction yielded similar results as measured one hour into a diet choice test. Potassium restriction, however, reversed the pattern: rats avoided the demonstrator’s diet but hamsters preferred it. Clearly, the valence of social information depended on the nutrient from which individuals were restricted and the species under study. This could be related to the contrasting social organization that members of each species generate. Neither species relied on social information about the availability of a nutrient from which they were restricted if they could taste that nutrient for themselves (sodium, carbohydrates).

Acute corticosterone sexually dimorphically facilitates social learning and inhibits feeding in mice

In numerous species social learning is predominant and adaptive, yet, we know little of its neurobiological mechanisms. Social learning is modulated by motivations and emotions, in a manner that is often sexually dimorphic. Additionally, stress hormones acutely modulate the related social cognitive process of social recognition. Whether this is true even for social learning is currently unknown. We investigated the acute effects of the stress hormone corticosterone (CORT) on the social transmission of food preferences (STFP) in male and female mice. During a brief social interaction an observer (OBS) acquires a food preference from a same-sex demonstrator (DEM). CORT (1.0, 2.5, 5.0 mg/kg), its ethanol vehicle (0.1%), and saline solution (0.9%) were administered intraperitoneally to the OBS, 10 min before a 30-min social interaction. Levels of plasma CORT were assessed in other mice that had received the same doses of CORT and either had or had not gone through a 30 min social interaction 10 min post-treatment. Exogenous CORT elicited levels of plasma level comparable to those seen at the peak of the circadian cycle and facilitated the STFP with males responding more than females both in terms of the duration of the food preference and the minimum effective dose. CORT also sexually dimorphically inhibited feeding, with females showing a greater dose–response than males. Saline solution and ethanol vehicles also sexually dimorphically facilitated the STFP and reduced feeding, but less than CORT did. These results indicate that CORT facilitates social learning, like social recognition. Hence, CORT may generally increase social information processing.

Food, “Culture,” and Sociality in Drosophila

GENERAL COMMENTARY article Front. Psychol., 28 May 2012Sec. Comparative Psychology https://doi.org/10.3389/fpsyg.2012.00165

Differential Effects of Estrogen Receptor Alpha and Beta Specific Agonists on Social Learning of Food Preferences in Female Mice

There is an evolutionary advantage to learning food preferences from conspecifics, as social learning allows an individual to bypass the risks associated with trial and error individual learning. The social transmission of food preferences (STFP) paradigm examines this advantage. Females in the proestrus and diestrus phases of the estrous cycle show a prolonged preference for the demonstrated food relative to estrus and ovariectomized females. Additionally, both estrogen receptor alpha (ERalpha) and estrogen receptor beta (ERbeta) knockout mice show impaired social recognition, which suggests that both receptors may be involved in other types of socially dependent learning, including the STFP. The present study investigated the effect of the ERalpha selective agonist PPT (1,3,5-tris(4-hydroxyphenyl)-4-propyl-1H-pyrazole) and the ERbeta selective agonist WAY-200070 (7-Bromo-2-(4-hydroxyphenyl)-1,3-benzoxazol-5-ol) on the STFP. Results showed that ovariectomized (ovx) mice treated with PPT failed to learn the socially acquired preference, while WAY-200070-treated ovx mice showed a two-fold prolonged preference for the food eaten by their demonstrator. The effects of PPT on the socially acquired food preference cannot be explained by effects on the total food intake of the groups or on the type of interaction with the demonstrator mouse. The effects of WAY-200070 may be partially due to effects on Submissive Behavior. The higher WAY-200070 doses produced prolonged preferences similar to those seen previously in intact female mice during the proestrus and diestrus phases. This suggests that the estrous cycle's effects on social learning may be due to the action of ERbeta on Submissive Behavior, or to ERbeta countering that of ERalpha.

Rapid forgetting of social transmission of food preferences in aged rats: Relationship to hippocampal CREB activation

A major characteristic of age-related changes in memory in rodents is an increase in the rate of forgetting of new information, even when tests given soon after training reveal intact memory. Interference with CREB functions similarly results in rapid decay of memory. Using quantitative immunocytochemistry, the present experiment examined the number of CREB- and pCREB-immunoreactive neurons in three regions of the dorsal and ventral hippocampus (dentate gyrus, CA3, and CA1) as a function of age and training. Rats were trained in a social transmission of food preference task. Using different food pairings, memory was tested in each rat immediately and 1, 2, 3, and 7 d later. Both young and old rats had intact and comparable memory scores at the immediate and 24-h tests, but old rats exhibited more rapid forgetting thereafter relative to that of young rats. The main findings were that training resulted in large increases in the number of pCREB-immunoreactive cells throughout the hippocampus in both young and aged rats. However, particularly in the ventral hippocampus, the training-elicited increase in pCREB-positive neurons was significantly lower in old than in young rats. Based on Western blot analyses in a separate set of rats, CREB levels were not responsive to training but were lower in the ventral hippocampus of old rats than of young rats. The present findings suggest that lower activation of CREB after training may contribute to the rapid forgetting seen in aged rats.

Dogs acquire food preferences from interacting with recently fed conspecifics

Social transmission of food preferences has been documented in many species including humans, rodents, and birds. In the current experiment, 12 pairs of domestic dogs (Canis familiaris) were utilized. Within each pair, one dog (the demonstrator) was fed dry dog food flavored with either basil or thyme. The second dog (the observer) interacted with one demonstrator for 10 min before being given an equal amount of both flavored foods. Observers exhibited a significant preference for the flavored diet consumed by their demonstrators, indicating that dogs, like rats, prefer foods smelled on a conspecific's breath.

Cognitive and neurological deficits induced by early and prolonged basal forebrain cholinergic hypofunction in rats

In the present study we examined the long-term effects of neonatal lesion of basal forebrain cholinergic neurons induced by intracerebroventricular injections of the immunotoxin 192 IgG saporin. Animals were then characterised behaviourally, electrophysiologically and molecularly. Cognitive effects were evaluated in the social transmission of food preferences, a non-spatial associative memory task. Electrophysiological effects were assessed by recording of cortical electroencephalographic (EEG) patterns. In addition, we measured the levels of proteins whose abnormal expression has been associated with neurodegeneration such as amyloid precursor protein (APP), presenilin 1 and 2 (PS-1, PS-2), and cyclooxygenases (COX-1 and COX-2). In animals lesioned on postnatal day 7 and tested 6 months thereafter, memory impairment in the social transmission of food preferences was evident, as well as a significant reduction of choline acetyltransferase activity in hippocampus and neocortex. Furthermore, similar to what observed in Alzheimer-like dementia, EEG cortical patterns in lesioned rats presented changes in α, β and δ activities. Levels of APP protein and mRNA were not affected by the treatment. Levels of hippocampal COX-2 protein and mRNA were significantly decreased whereas COX-1 remained unaltered. PS-1 and PS-2 transcripts were reduced in hippocampus and neocortex. These findings indicate that neonatal and permanent basal forebrain cholinergic hypofunction is sufficient to induce behavioural and neuropathological abnormalities. This animal model could represent a valid tool to evaluate the role played by abnormal cholinergic maturation in later vulnerability to neuropathological processes associated with cognitive decline and, possibly, to Alzheimer-like dementia.

Loss of Ca2+/Calmodulin Kinase Kinase β Affects the Formation of Some, But Not All, Types of Hippocampus-Dependent Long-Term Memory

Long-term memory (LTM) requires activation of the transcription factor cAMP-responsive element binding protein (CREB). Signaling by the Ca2+/calmodulin (CaM) kinase cascade has been implicated in CREB activation and memory consolidation processes in the hippocampus. The CaM kinase kinase beta isoforms belong to the CaM kinase cascade, and we have generated null mutant mice to investigate the role of these kinases in several forms of learning and memory. The null mutants were impaired in spatial training-induced CREB activation and spatial memory formation. Furthermore, the mutants lacked late, but not early, long-term potentiation at the hippocampal CA1 synapse, and they were impaired in LTM, but not short-term memory, for the social transmission of food preferences. We suggest that the CaM kinase kinasebeta isoforms are required for the formation of hippocampal LTM. Surprisingly, however, these kinases were not needed for contextual, trace fear, and passive avoidance LTM. Our results demonstrate that different signaling processes underlie the formation of these types of hippocampal LTM.

Social transmission and memory of food preferences in pine voles (Microtus pinetorum).

The social transmission of food preferences is affected by factors including the length of time a preference is maintained. The authors investigated the social transmission of food preferences in pine voles (Microtus pinetorum) and whether food items had to be present for memory to persist. A demonstrator vole was fed cocoa-flavored food, a nonpreferred food. After interacting with a demonstrator vole, observer voles preferred cocoa-flavored food as compared with either naive voles that had not interacted with demonstrators or voles that had been exposed to odors. Observers retained this preference for 72 hr after interacting with an observer whether or not flavored foods were present. The ability to learn which food items are palatable and safe may benefit a generalist herbivore that has faced selection to avoid toxic baits.

Hippocampus-dependent learning and memory is impaired in mice lacking the Ras-guanine-nucleotide releasing factor 1 (Ras-GRF1)

Previous results have suggested that the Ras signaling pathway is involved in learning and memory. Ras is activated by nucleotide exchange factors, such as the calmodulin-activated guanine-nucleotide releasing factor 1 (Ras-GRF1). To test whether Ras-GRF1 is required for learning and memory, we inactivated the Ras-GRF1 gene in mice. These mutants performed normally in a rota-rod motor coordination task, and in two amygdala-dependent tasks (inhibitory avoidance and contextual conditioning). In contrast the mutants were impaired in three hippocampus-dependent learning tasks: contextual discrimination, the social transmission of food preferences, and the hidden-platform version of the Morris water maze. These studies indicate that Ras-GRF1 plays a role in hippocampal-dependent learning and memory.

Cholinergic basal forebrain is critical for social transmission of food preferences.

Studies using selective lesions of basal forebrain cholinergic neurons suggest that these neurons play a role in attentional processing, but not learning and memory. However, the tests of learning and memory used thus far have been restricted largely to spatial tasks. In the present study, we examined whether the cholinergic basal forebrain plays a role in a form of nonspatial associative memory, the social transmission of food preferences. Sham-operated control rats were compared to rats with 192 IgG-saporin lesions of the medial septum/diagonal band cholinergic projections to hippocampus or nucleus basalis magnocellularis/substantia innominata cholinergic projections to neocortex. Both lesions impaired 24-h retention of a learned social food preference relative to controls, despite performance on an immediate retention trial that was indistinguishable from controls. Moreover, 24-h retention of the socially learned food preference correlated strongly with cholinergic enzymatic activity in the neocortex, but not in the hippocampus. Immunohistochemical data confirmed significant and selective lesion-induced cholinergic depletions in the intended brain regions. These data provide evidence that the cholinergic basal forebrain, particularly the cholinergic projection to neocortex, is involved in the formation and/or retrieval of social memories related to food preference, and suggest a role for cortical acetylcholine in consolidation of associative memory processes.