A bird's eye view of the hippocampus beyond space: Behavioral, neuroanatomical, and neuroendocrine perspectives.

Although the hippocampus is one of the most-studied brain regions in mammals, research on the avian hippocampus has been more limited in scope. It is generally agreed that the hippocampus is an ancient feature of the amniote brain, and therefore homologous between the two lineages. Because birds and mammals are evolutionarily not very closely related, any shared anatomy is likely to be crucial for shared functions of their hippocampi. These functions, in turn, are likely to be essential if they have been conserved for over 300 million years. Therefore, research on the avian hippocampus can help us understand how this brain region evolved and how it has changed over evolutionary time. Further, there is a strong research foundation in birds on hippocampal-supported behaviors such as spatial navigation, food caching, and brood parasitism that scientists can build upon to better understand how hippocampal anatomy, network circuitry, endocrinology, and physiology can help control these behaviors. In this review, we summarize our current understanding of the avian hippocampus in spatial cognition as well as in regulating anxiety, approach-avoidance behavior, and stress responses. Although there are still some questions about the exact number of subdivisions in the avian hippocampus and how that might vary in different avian families, there is intriguing evidence that the avian hippocampus might have complementary functional profiles along the rostral-caudal axis similar to the dorsal-ventral axis of the rodent hippocampus, where the rostral/dorsal hippocampus is more involved in cognitive processes like spatial learning and the caudal/ventral hippocampus regulates emotional states, anxiety, and the stress response. Future research should focus on elucidating the cellular and molecular mechanisms - including endocrinological - in the avian hippocampus that underlie behaviors such as spatial navigation, spatial memory, and anxiety-related behaviors, and in so doing, resolve outstanding questions about avian hippocampal function and organization.

Different memory systems in food-hoarding birds: A response to Pravosudov.

We recently showed that food-hoarding birds use familiarity processes more than recollection processes when remembering the spatial location of their caches (Smulders et al., Animal Cognition 26:1929-1943, 2023). Pravosudov (Learning & Behavior, https://doi.org/ https://doi.org/10.3758/s13420-023-00616-x , 2023) called our findings into question, claiming that our method is unable to distinguish between recollection and familiarity, and that associative learning tasks are a better way to study the memory for cache sites. In this response, we argue that our methods would have been more likely to detect recollection than familiarity, if Pravosudov's assertions were correct. We also point out that associative learning mechanisms may be good for building semantic knowledge, but are incompatible with the needs of cache site memory, which requires the unique encoding of caching events.

Identifying the nature of episodic memory deficits in Major Depressive Disorder using a Real-World What-Where-When task.

ABSTRACTDeficits in episodic memory have been reported in various psychiatric conditions, including Major Depressive Disorder (MDD). Many widely used episodic memory tests do not have the ability to distinguish between impaired memory of separate components of a real-life event (e.g., what happened, where it happened and when), and impaired binding of such real-life features. To address this issue, a naturalistic, real-world What-Where-When memory task was employed to assess the nature of episodic memory impairments in MDD. A validation study established that the task is sensitive to age-related episodic memory changes, and that intentional encoding does not invalidate the task. The main study then compared the performance of patients with depression and control participants on the intentionally encoded WWW task. Patients with MDD presented an overall episodic memory impairment arising from deficits in object memory and the ability to bind objects to temporal context. Taken together, our study confirms the episodic memory impairment in MDD, by providing evidence of deficient object memory and reduced ability to bind temporal context to objects in patients. Our naturalistic WWW task presents a promising approach for thorough identification of the nature of episodic memory impairments, under a real-world environment, in various conditions, including MDD.

Hoarding titmice predominantly use Familiarity, and not Recollection, when remembering cache locations.

Scatter-hoarding birds find their caches using spatial memory and have an enlarged hippocampus. Finding a cache site could be achieved using either Recollection (a discrete recalling of previously experienced information) or Familiarity (a feeling of "having encountered something before"). In humans, these two processes can be distinguished using receiver operating characteristic (ROC) curves. ROC curves for olfactory memory in rats have shown the hippocampus is involved in Recollection, but not Familiarity. We test the hypothesis that food-hoarding birds, having a larger hippocampus, primarily use Recollection to find their caches. We validate a novel method of constructing ROC curves in humans and apply this method to cache retrieval by coal tits (Periparus ater). Both humans and birds mainly use Familiarity in finding their caches, with lower contribution of Recollection. This contribution is not significantly different from chance in birds, but a small contribution cannot be ruled out. Memory performance decreases with increasing retention interval in birds. The ecology of food-hoarding Parids makes it plausible that they mainly use Familiarity in the memory for caches. The larger hippocampus could be related to associating cache contents and temporal context with cache locations, rather than Recollection of the spatial information itself.

Seasonal changes in the hippocampal formation of hoarding and non-hoarding tits.

The hippocampal formation (HF) processes spatial memories for cache locations in food-hoarding birds. Hoarding is a seasonal behavior, and seasonal changes in the HF have been described in some studies, but not in others. One potential reason is that birds may have been sampled during the seasonal hoarding peak in some studies, but not in others. In this study, we investigate the seasonal changes in hoarding and HF in willow tits (Poecile montanus). We compare this to seasonal changes in HF in a closely related non-hoarding bird, the great tit (Parus major). Willow tits near Oulu, Finland, show a seasonal hoarding peak in September and both HF volume and neuron number show a similar peak. HF neuronal density also increases in September, but then remains the same throughout winter. Unexpectedly, the great tit HF also changes seasonally, although in a different pattern: the great tit telencephalon increases in volume from July to August and decreases again in November. Great tit HF volume follows suit, but with a delay. Great tit HF neuron number and density also increase from August to September and stay high throughout winter. We hypothesize that seasonal changes in hoarding birds' HF are driven by food-hoarding experience (e.g., the formation of thousands of memories). The seasonal changes in great tit brains may also be due to experience-dependent plasticity, responding to changes in the social and spatial environment. Large-scale experience-dependent neural plasticity is therefore probably not an adaptation of food-hoarding birds, but a general property of the avian HF and telencephalon.

Smarter through group living?

Wild Australian magpies living (or growing up) in larger social groups take fewer trials to solve a battery of four cognitive tests than those living (or growing up) in smaller groups. The tests all draw on a common underlying factor, but is this factor cognitive or motivational?

"How Foraging Works": Let's not forget the physiological mechanisms of energy balance.

Anselme & Güntürkün propose a novel mechanism to explain the increase in foraging motivation when experiencing an unpredictable food supply. However, the physiological mechanisms that maintain energy homeostasis already control foraging intensity in response to changes in energy balance. Therefore, unpredictability may just be one of many factors that feeds into the same dopaminergic "wanting" system to control foraging intensity.

In vitro characterization of gamma oscillations in the hippocampal formation of the domestic chick.

Avian and mammalian brains have evolved independently from each other for about 300 million years. During that time, the hippocampal formation (HF) has diverged in morphology and cytoarchitecture, but seems to have conserved much of its function. It is therefore an open question how seemingly different neural organizations can generate the same function. A prominent feature of the mammalian hippocampus is that it generates different neural oscillations, including the gamma rhythm, which plays an important role in memory processing. In this study, we investigate whether the avian hippocampus also generates gamma oscillations, and whether similar pharmacological mechanisms are involved in this function. We investigated the existence of gamma oscillations in avian HF using in vitro electrophysiology in P0-P12 domestic chick (Gallus gallus domesticus) HF brain slices. Persistent gamma frequency oscillations were induced by the bath application of the cholinergic agonist carbachol, but not by kainate, a glutamate receptor agonist. Similar to other species, carbachol-evoked gamma oscillations were sensitive to GABAA , AMPA/kainate and muscarinic (M1) receptor antagonism. Therefore, similar to mammalian species, muscarinic receptor-activated avian HF gamma oscillations may arise via a pyramidal-interneuron gamma (PING)-based mechanism. Gamma oscillations are most prominent in the ventromedial area of the hippocampal slices, and gamma power is reduced more laterally and dorsally in the HF. We conclude that similar micro-circuitry may exist in the avian and mammalian hippocampal formation, and this is likely to relate to the shared function of the two structures.

Peripherally injected ghrelin and leptin reduce food hoarding and mass gain in the coal tit (Periparus ater).

In birds little is known about the hormonal signals that communicate nutritional state to the brain and regulate appetitive behaviours. In mammals, the peptide hormones ghrelin and leptin elevate and inhibit consumption and food hoarding, respectively. But in birds, administration of both ghrelin and leptin inhibit food consumption. The role of these hormones in the regulation of food hoarding in avian species has not been examined. To investigate this, we injected wild caught coal tits (Periparus ater) with leptin, high-dose ghrelin, low-dose ghrelin and a saline control in the laboratory. We then measured food hoarding and mass gain, as a proxy of food consumption, every 20 min for 2 h post-injection. Both high-dose ghrelin and leptin injections significantly reduced hoarding and mass gain compared with controls. Our results provide the first evidence that hoarding behaviour can be reduced by both leptin and ghrelin in a wild bird. These findings add to evidence that the hormonal control of food consumption and hoarding in avian species differs from that in mammals. Food hoarding and consumptive behaviours consistently show the same response to peripheral signals of nutritional state, suggesting that the hormonal regulation of food hoarding has evolved from the consumption regulatory system.

The Avian Hippocampal Formation and the Stress Response.

Though widely studied for its function in memory and navigation, the hippocampal formation (HF) in mammals also plays an important role in regulating the stress response. If this is an ancestral feature of the hippocampus, then it is likely that the avian HF plays a similar role. Indeed, the avian HF strongly expresses both mineralocorticoid and glucocorticoid receptors, and has indirect projections to the paraventricular nucleus of the hypothalamus, which controls the hypothalamic-pituitary-adrenal (HPA) axis. Hippocampal lesions increase HPA activity, while electrical stimulation suppresses it. In addition, adult hippocampal neurogenesis in birds is reduced in response to different acute and chronic stressors, as it is in mammals. Because the mammalian hippocampus is functionally specialized along its septotemporal axis, with the temporal pole playing a more important role in the stress response, the hypothesis is put forward that a similar functional specialization exists in birds along the rostrocaudal hippocampal axis. Some, though not all, of the evidence supports a rostrocaudal functional gradient. The evidence for whether this is equivalent to the mammalian septotemporal organization is currently ambiguous at best and needs to be more extensively investigated.

How does intentionality of encoding affect memory for episodic information?

Episodic memory enables the detailed and vivid recall of past events, including target and wider contextual information. In this paper, we investigated whether/how encoding intentionality affects the retention of target and contextual episodic information from a novel experience. Healthy adults performed (1) a What-Where-When (WWW) episodic memory task involving the hiding and delayed recall of a number of items (what) in different locations (where) in temporally distinct sessions (when) and (2) unexpected tests probing memory for wider contextual information from the WWW task. Critically, some participants were informed that memory for WWW information would be subsequently probed (intentional group), while this came as a surprise for others (incidental group). The probing of contextual information came as a surprise for all participants. Participants also performed several measures of episodic and nonepisodic cognition from which common episodic and nonepisodic factors were extracted. Memory for target (WWW) and contextual information was superior in the intentional group compared with the incidental group. Memory for target and contextual information was unrelated to factors of nonepisodic cognition, irrespective of encoding intentionality. In addition, memory for target information was unrelated to factors of episodic cognition. However, memory for wider contextual information was related to some factors of episodic cognition, and these relationships differed between the intentional and incidental groups. Our results lead us to propose the hypothesis that intentional encoding of episodic information increases the coherence of the representation of the context in which the episode took place. This hypothesis remains to be tested.

Different Seasonal Patterns in Song System Volume in Willow Tits and Great Tits.

In most species of seasonally breeding songbirds studied to date, the brain areas that control singing (i.e. the song control system, SCS) are larger during the breeding season than at other times of the year. In the family of titmice and chickadees (Paridae), one species, the blue tit (Cyanistes caeruleus), shows the typical pattern of seasonal changes, while another species, the black-capped chickadee (Poecile atricapillus), shows, at best, very reduced seasonal changes in the SCS. To test whether this pattern holds up in the two Parid lineages to which these two species belong, and to rule out that the differences in seasonal patterns observed were due to differences in geography or laboratory, we compared the seasonal patterns in two song system nuclei volumes (HVC and Area X) in willow tits (Poecile montanus), closely related to black-capped chickadees, and in great tits (Parus major), more closely related to blue tits, from the same area around Oulu, Finland. Both species had larger gonads in spring than during the rest of the year. Great tit males had a larger HVC in spring than at other times of the year, but their Area X did not change in size. Willow tits showed no seasonal change in HVC or Area X size, despite having much larger gonads in spring than the great tits. Our findings suggest that the song system of willow tits and their relatives may be involved in learning and producing nonsong social vocalizations. Since these vocalizations are used year-round, there may be a year-round demand on the song system. The great tit and blue tit HVC may change seasonally because the demand is only placed on the song system during the breeding season, since they only produce learned vocalizations during this time. We suggest that changes were not observed in Area X because its main role is in song learning, and there is evidence that great tits do not learn new songs after their first year of life. Further study is required to determine whether our hypothesis about the role of the song system in the learned, nonsong vocalizations of the willow tit and chickadee is correct, and to test our hypothesis about the role of Area X in the great tit song system.

Viewing 3D TV over two months produces no discernible effects on balance, coordination or eyesight.

With the rise in stereoscopic 3D media, there has been concern that viewing stereoscopic 3D (S3D) content could have long-term adverse effects, but little data are available. In the first study to address this, 28 households who did not currently own a 3D TV were given a new TV set, either S3D or 2D. The 116 members of these households all underwent tests of balance, coordination and eyesight, both before they received their new TV set, and after they had owned it for 2 months. We did not detect any changes which appeared to be associated with viewing 3D TV. We conclude that viewing 3D TV does not produce detectable effects on balance, coordination or eyesight over the timescale studied. Practitioner Summary: Concern has been expressed over possible long-term effects of stereoscopic 3D (S3D). We looked for any changes in vision, balance and coordination associated with normal home S3D TV viewing in the 2 months after first acquiring a 3D TV. We find no evidence of any changes over this timescale.

Stereoscopic 3-D content appears relatively veridical when viewed from an oblique angle.

Geometrically, stereoscopic 3-D (S3D) content should appear distorted unless viewed from the position for which the content was produced. Almost all commercial and laboratory S3D content is generated assuming that it will be presented on a screen frontoparallel to the viewer. However, in cinema and the home, S3D content is regularly viewed from oblique angles, and yet shapes are not usually perceived to be distorted. It is not yet known whether this is simply because viewers are insensitive to incorrect viewing angles or because viewers automatically compensate for oblique viewing, as they do for 2-D content. Here, we investigate this using a canonical-form paradigm. We show that S3D content can indeed appear warped when viewed from oblique angles, and that this effect is more pronounced than for 2-D content. We hypothesized that motion cues in the content would aid in the correct perception of S3D content, making it appear more natural even when viewed obliquely, but we find little support for this idea. However, the perceptual distortions are still small, and viewers do compensate to some extent for oblique viewing. We conclude that, at least as regards object distortion, oblique viewing is unlikely to be substantially more of a problem for S3D content than it already is for 2-D.

Different mechanisms are responsible for dishabituation of electrophysiological auditory responses to a change in acoustic identity than to a change in stimulus location.

Repeated exposure to an auditory stimulus leads to habituation of the electrophysiological and immediate-early-gene (IEG) expression response in the auditory system. A novel auditory stimulus reinstates this response in a form of dishabituation. This has been interpreted as the start of new memory formation for this novel stimulus. Changes in the location of an otherwise identical auditory stimulus can also dishabituate the IEG expression response. This has been interpreted as an integration of stimulus identity and stimulus location into a single auditory object, encoded in the firing patterns of the auditory system. In this study, we further tested this hypothesis. Using chronic multi-electrode arrays to record multi-unit activity from the auditory system of awake and behaving zebra finches, we found that habituation occurs to repeated exposure to the same song and dishabituation with a novel song, similar to that described in head-fixed, restrained animals. A large proportion of recording sites also showed dishabituation when the same auditory stimulus was moved to a novel location. However, when the song was randomly moved among 8 interleaved locations, habituation occurred independently of the continuous changes in location. In contrast, when 8 different auditory stimuli were interleaved all from the same location, a separate habituation occurred to each stimulus. This result suggests that neuronal memories of the acoustic identity and spatial location are different, and that allocentric location of a stimulus is not encoded as part of the memory for an auditory object, while its acoustic properties are. We speculate that, instead, the dishabituation that occurs with a change from a stable location of a sound is due to the unexpectedness of the location change, and might be due to different underlying mechanisms than the dishabituation and separate habituations to different acoustic stimuli.

Water-induced finger wrinkles improve handling of wet objects.

Upon continued submersion in water, the glabrous skin on human hands and feet forms wrinkles. The formation of these wrinkles is known to be an active process, controlled by the autonomic nervous system. Such an active control suggests that these wrinkles may have an important function, but this function has not been clear. In this study, we show that submerged objects are handled more quickly with wrinkled fingers than with unwrinkled fingers, whereas wrinkles make no difference to manipulating dry objects. These findings support the hypothesis that water-induced finger wrinkles improve handling submerged objects and suggest that they may be an adaptation for handling objects in wet conditions.

Magpies can use local cues to retrieve their food caches.

Much importance has been placed on the use of spatial cues by food-hoarding birds in the retrieval of their caches. In this study, we investigate whether food-hoarding birds can be trained to use local cues ("beacons") in their cache retrieval. We test magpies (Pica pica) in an active hoarding-retrieval paradigm, where local cues are always reliable, while spatial cues are not. Our results show that the birds use the local cues to retrieve their caches, even when occasionally contradicting spatial information is available. The design of our study does not allow us to test rigorously whether the birds prefer using local over spatial cues, nor to investigate the process through which they learn to use local cues. We furthermore provide evidence that magpies develop landmark preferences, which improve their retrieval accuracy. Our findings support the hypothesis that birds are flexible in their use of memory information, using a combination of the most reliable or salient information to retrieve their caches.

Do humans use episodic memory to solve a What-Where-When memory task?

What-Where-When (WWW) memory tasks have been used to study episodic(-like) memory in non-human animals. In this study, we investigate whether humans use episodic memory to solve such a WWW memory task. Participants are assigned to one of two treatments, in which they hide different coin types (what) in different locations (where) on two separate occasions (when). In the Active treatment, which mimics the animal situation as closely as possible, participants are instructed to memorize the WWW information; in the Passive treatment, participants are unaware of the fact that memory will be tested. In both groups, the majority of participants report using a mental time travel strategy to solve the task, and performance on a different episodic memory test significantly predicts performance on the WWW memory task. This suggests that the WWW memory task is a good test of episodic memory in humans. Participants remember locations and coins from the first hiding session better than they do those of the second hiding session, suggesting their memories may be reinforced during the second hiding session. We also investigated how well episodic memory performance predicted performance on the three aspects of the WWW memory task separately. In the Passive treatment, episodic memory performance predicts performance on all three aspects of the WWW memory task equally. However, in the Active treatment it only predicts performance on the what component. This could imply that during active encoding a different memory system is used for where and when information than during passive encoding. Encoding of what information seems to rely on episodic memory processing in both conditions.

Telencephalic regulation of the HPA axis in birds.

The hypothalamo-pituitary-adrenal (HPA) axis is one of the major output systems of the vertebrate stress response. It controls the release of cortisol or corticosterone from the adrenal gland. These hormones regulate a range of processes throughout the brain and body, with the main function of mobilizing energy reserves to improve coping with a stressful situation. This axis is regulated in response to both physical (e.g., osmotic) and psychological (e.g., social) stressors. In mammals, the telencephalon plays an important role in the regulation of the HPA axis response in particular to psychological stressors, with the amygdala and part of prefrontal cortex stimulating the stress response, and the hippocampus and another part of prefrontal cortex inhibiting the response to return it to baseline. Birds also mount HPA axis responses to psychological stressors, but much less is known about the telencephalic areas that control this response. This review summarizes which telencephalic areas in birds are connected to the HPA axis and are known to respond to stressful situations. The conclusion is that the telencephalic control of the HPA axis is probably an ancient system that dates from before the split between sauropsid and synapsid reptiles, but more research is needed into the functional relationships between the brain areas reviewed in birds if we want to understand the level of this conservation.