Microbiota and stress: a loop that impacts memory.

Chronic stress and the gut microbiota appear to comprise a feed-forward loop, which contributes to the development of depressive disorders. Evidence suggests that memory can also be impaired by either chronic stress or microbiota imbalance. However, it remains to be established whether these could be a part of an integrated loop model and be responsible for memory impairments. To shed light on this, we used a two-pronged approach in Japanese quail: first stress-induced alterations in gut microbiota were characterized, then we tested whether this altered microbiota could affect brain and memory function when transferred to a germ-free host. The cecal microbiota of chronically stressed quails was found to be significantly different from that of unstressed individuals with lower α and ß diversities and increased Bacteroidetes abundance largely represented by the Alistipes genus, a well-known stress target in rodents and humans. The transfer of this altered microbiota into germ-free quails decreased their spatial and cue-based memory abilities as previously demonstrated in the stressed donors. The recipients also displayed increased anxiety-like behavior, reduced basal plasma corticosterone levels and differential gene expression in the brain. Furthermore, cecal microbiota transfer from a chronically stressed individual was sufficient to mimic the adverse impact of chronic stress on memory in recipient hosts and this action may be related to the Alistipes genus. Our results provide evidence of a feed-forward loop system linking the microbiota-gut-brain axis to stress and memory function and suggest that maintaining a healthy microbiota could help alleviate memory impairments linked to chronic stress.

Training level reveals a dynamic dialogue between stress and memory systems in birds.

Chronic stress profoundly affects forms of declarative memory, such as spatial memory, while it may spare non-declarative memory, such as cue-based memory. It is known, however, that the effects of chronic stress on memory systems may vary according to the level of training of an individual was submitted. Here, we investigated, in birds, how chronic stress impact spatial and cue-based memories according to training level. For that, control and chronically stressed Japanese quail were trained in a task that could be solved using spatial and cue-based memory and tested for their memory performance after 5 and 15 training days (initial training and overtraining, respectively) and following an emotional challenge (exposure to an open field). Our results showed that, compared to control quail, chronic stress impacted negatively spatial memory performances in stressed birds after initial training, but these differences were lowered after overtraining. Control birds seemed to shift from spatial to cue-based memory to solve the task across overtraining. However, an emotional challenge before testing reinstated the negative impact of chronic stress on spatial memory performances between the groups, revealing that chronic stress/overtraining did not eliminate the spatial memory and differences caused by stressors can reemerge depending on the individual's immediate psychological state. Contrary to spatial memory, cue-based memory was not affected in chronically stressed birds compared to control birds in any test occasion, confirming its resistance against the negative effects of chronic stress. Altogether these findings reveal a dynamic dialogue between stress, training level, and memory systems in birds.

Emotionality modulates the impact of chronic stress on memory and neurogenesis in birds.

Chronic stress is a strong modulator of cognitive processes, such as learning and memory. There is, however, great within-individual variation in how an animal perceives and reacts to stressors. These differences in coping with stress modulate the development of stress-induced memory alterations. The present study investigated whether and how chronic stress and individual emotionality interrelate and influence memory performances and brain neurogenesis in birds. For that, we used two lines of Japanese quail (Coturnix japonica) with divergent emotionality levels. Highly (E+) and less (E-) emotional quail were submitted to chronic unpredictable stress (CUS) for 3 weeks and trained in a spatial task and a discrimination task, a form of cue-based memory. E + and E- birds were also used to assess the impact of CUS and emotionality on neurogenesis within the hippocampus and the striatum. CUS negatively impacted spatial memory, and cell proliferation, and survival in the hippocampus. High emotionality was associated with a decreased hippocampal neurogenesis. CUS improved discrimination performances and favored the differentiation of newborn cells into mature neurons in the striatum, specifically in E+ birds. Our results provide evidence that CUS consequences on memory and neural plasticity depends both on the memory system and individual differences in behavior.

Research Note: Role of the hippocampus in spatial memory in Japanese quail.

The Japanese quail is a powerful model to characterize behavioral, physiological, and neurobiological processes in Galliformes. Behavioral tests have already been adapted for quail to assess memory systems, but despite the pivotal role of the hippocampus in this cognitive process, its involvement in spatial memory has not been demonstrated in this species. In this study, lesions were created in the hippocampus of Japanese quail, and both lesioned and control quail were tested for spatial and cue-based learning performances. These hippocampal lesions specifically impacted spatial learning performance, but spared learning performance when birds could solve the task using their cue-based memory. These findings, thus, highlight that the hippocampus plays a crucial role and is essential for spatial declarative memory. Future studies could aim to elucidate the cellular or molecular mechanisms involved in this form of memory.

Social motivation and the use of distal, but not local, featural cues are related to ranging behavior in free-range chickens (Gallus gallus domesticus).

Animals can navigate an environment relying on different sources of information, such as geometrical or featural cues. The favoring of one type of information over another depends on multiple factors, such as inter-individual differences in behavior and cognition. Free-range chickens present different range use patterns, which may be explained by behavioral and cognitive differences. However, how behavior, cognition, and range use intercorrelate is still poorly understood. In this work, we aimed to further understand possible differences in behavior and cognition between two groups of free-range broiler chickens: those who frequently explore their range ('high rangers') and those who prefer to stay in or near the barn ('low rangers'). Prior to range access, individual behavior was measured in open field-, emergence-, and social motivation tests. To investigate cognitive differences, we analyzed whether exploratory behavior was linked to different performances in the use of distal and local spatial cues during an orientation task. During the social motivation test, low rangers showed a higher inclination to be near conspecifics than did high rangers. Our orientation tests show that chickens preferred to orientate themselves using the local cues over the distal cues. Individual differences were only found for distal, but not for local, cue use suggesting that demanding tasks are more efficient in revealing individual cognitive differences. Our results suggest that considering variation in social motivation may allow a more comprehensive understanding of chicken range use. Our results also support the importance of incorporating multiple aspects of individual differences to understand individual reactions to its environment.

Horses prefer to solicit a person who previously observed a food-hiding process to access this food: A possible indication of attentional state attribution.

Inferring what others witnessed provides important benefits in social contexts, but evidence remains scarce in nonhuman animals. We investigated this ability in domestic horses by testing whether they could discriminate between two experimenters who differed in what they previously witnessed and decide whom to solicit when confronted with an unreachable food source based on that information. First, horses saw food being hidden in a closed bucket (impossible for them to open) in the presence of two experimenters who behaved identically but differed in their attention to the baiting process (the "witness" experimenter faced the bucket, the "non-witness" faced away). Horses were then let free with both experimenters, and their interest towards each (gaze and touch) was measured. They gazed at and touched the witness significantly more than the non-witness (n = 15, gaze: p = 0.004; touch: p = 0.003). These results might suggest that horses inferred the attentional state of the experimenters during the baiting process and used this information to adapt their later behavior. Although further study would be necessary to conclude, our study provides new insight into attentional state attribution in horses and might hint to the existence of precursors of a Theory of Mind in horses.

Relationship between ranging behavior and spatial memory of free-range chickens.

Different personalities may lead to different ways of processing environmental information; however, the relationship between personality and cognition is not fully understood as studies on diverse species present contrasting results. As there is great within-flock variability of outdoor ranging behavior in free-range broiler chickens, we tested whether and how ranging behavior impacts on individual spatial memory abilities. The experiment was conducted on one flock (n = 200) reared in the same conditions throughout the study, to simulate on-farm situations. As the ranging behavior was stable over time, we compared two distinct groups of male chickens: one that visited the range more (High rangers) and one that was more prone to staying in the poultry house (Low rangers). To test the spatial memory, individuals (n = 30) went through two main phases in an arena with 8 cups. For the familiarization phase, individuals were submitted to one trial per day, for seven days, to a situation where all eight cups were baited with mealworms. Animals had to reach a criterion of 5 cups visited out of 8 to advance to the next phase. For the spatial test, only four cups were baited and systematically placed at the same location. This last phase comprised two trials per individual per day, for nine days. During these two phases, latency to visit cups and the number of visits and revisits of all cups were recorded. Low ranger chickens took less time to attain the pre-established threshold of visiting 5 cups out of 8, over the familiarization phase. During the spatial test, the latency to visit four cups decreased between the within-day trials for low ranger chickens and increased for high ranger chickens. Moreover, in the within-day trial analysis, low ranger chickens exhibited an improvement on spatial memory and better spatial memory compared to high ranger chickens. Different speed-accuracy trade-offs may explain these differences between low and high ranger chickens and the way individuals interact and solve the task. Our study strengthens the scientific evidence relating consistent individual differences in behavior, with the ranging behavior of free-range chickens, and cognitive performance during a spatial memory task.

A trait for a high emotionality favors spatial memory to the detriment of cue-based memory in Japanese quail.

Recent studies provided evidence that a personality trait such as a trait for a high or a low emotionality can either promotes or impairs learning and memory performances. This variability can be partly explained because this trait may have opposite effect on memory performances depending on the memory system involved. The present study investigated in Japanese quail the relationships between emotionality and two forms of memory, spatial- memory and cue-based memory. We showed that birds with a high emotionality trait (E+), compared with birds with a low emotionality trait (E-), reached slowly but more accurately the spatial location of a rewarded cup in an arena that contains 8 identical cups. Then a second cohort of E + and E- quails was trained to solve a dual spatial/cued task in which they could use either their spatial or cue-based memory. Whereas E + birds predominantly solved the task using their spatial memory, E- birds preferentially used their cue-based memory. These findings demonstrate that a trait for a high emotionality, can influence spatial memory performances but also contributes to favor the selection of this form of memory.

Cyclic nucleotide-gated channels, calmodulin, adenylyl cyclase, and calcium/calmodulin-dependent protein kinase II are required for late, but not early, long-term memory formation in the honeybee.

Memory is a dynamic process that allows encoding, storage, and retrieval of information acquired through individual experience. In the honeybee Apis mellifera, olfactory conditioning of the proboscis extension response (PER) has shown that besides short-term memory (STM) and mid-term memory (MTM), two phases of long-term memory (LTM) are formed upon multiple-trial conditioning: an early phase (e-LTM) which depends on translation from already available mRNA, and a late phase (l-LTM) which requires de novo transcription and translation. Here we combined olfactory PER conditioning and neuropharmacological inhibition and studied the involvement of the NO-cGMP pathway, and of specific molecules, such as cyclic nucleotide-gated channels (CNG), calmodulin (CaM), adenylyl cyclase (AC), and Ca(2+)/calmodulin-dependent protein kinase (CaMKII), in the formation of olfactory LTM in bees. We show that in addition to NO-cGMP and cAMP-PKA, CNG channels, CaM, AC, and CaMKII also participate in the formation of a l-LTM (72-h post-conditioning) that is specific for the learned odor. Importantly, the same molecules are dispensable for olfactory learning and for the formation of both MTM (in the minute and hour range) and e-LTM (24-h post-conditioning), thus suggesting that the signaling pathways leading to l-LTM or e-LTM involve different molecular actors.