Socially-mediated activation in the snake social-decision-making network.

Brain areas important for social perception, social reward, and social behavior - collectively referred to as the social-decision-making network (SDN) - appear to be highly conserved across taxa. These brain areas facilitate a variety of social behaviors such as conspecific approach/avoidance, aggression, mating, parental care, and recognition. Although the SDN has been investigated across taxa, little is known about its functioning in reptiles. Research on the snake SDN may provide important new insights, as snakes have a keen social perceptual system and express a relatively reduced repertoire of social behaviors. Here, we present the results of an experiment in which ball pythons (Python regius) interacted with a same-sex conspecific for one hour and neural activation was investigated through Fos immunoreactivity. Compared to controls, snakes that interacted socially had higher Fos counts in brain areas implicated in social behavior across taxa, such as the medial amygdala, preoptic area, nucleus accumbens, and basolateral amygdala. Additionally, we found differential Fos immunoreactivity in the ventral amygdala, which facilitates communication between social brain areas. In many of these areas, Fos counts differed by sex, which may be due to increased competition between males. Fos counts did not differ in early sensory (i.e., vomeronasal) processing structures. As ball python social systems lack parental care, cooperation, or long-term group living, these results provide valuable insight into the basal functions of the vertebrate social decision-making network.

Altered pattern separation in Goto-Kakizaki rats.

Type 2 diabetes mellitus has steadily increased in prevalence over the past five decades. Among the health risks associated with this disorder are cognitive decline and are increased risk of developing dementia. To further investigate the link between diabetes and cognition, here we test memory performance and hippocampal function in the Goto-Kakizaki (GK) rat, a robust model of diabetes. Relative to age-matched Wistar rats, GK rats show impairments in a conjunctive memory task that requires discriminating objects not only on the basis of their physical characteristics, but also on the basis of where and when they were last seen. Concomitant to these deficits are changes in the pattern of expression of Egr1 (an immediate-early gene critical for memory) in dentate gyrus granule cells, consistent with dentate hypoactivity leading to unstable hippocampal representations. These data support the hypothesis that diabetes confers a phenotype of accelerated senescence on the hippocampus, and help to link this disorder with changes in hippocampal circuits.

A search pattern for the engram.

Roy and colleagues (Nature Communications, 13.1, 1-16, 2022) examined neuronal ensembles associated with contextual fear conditioning memory across multiple brain regions, referred to as a unified engram complex. Their four-step approach incorporating brain-wide mapping of activated neurons, engram indexing, and optogenetic and chemogenetic manipulations could offer a novel, holistic approach to implement in our continued search for the engram.

Functional dissociation along the rostrocaudal axis of Japanese quail hippocampus.

The mammalian hippocampus (Hp) can be functionally segregated along its septotemporal axis, with involvement of dorsal hippocampus (dHp) in spatial memory and ventral hippocampus (vHp) in stress responses and emotional behaviour. In the present study, we investigate comparable functional segregation in proposed homologues within the avian brain. Using Japanese quail (Coturnix Japonica), we report that bilateral lesions of the rostral hippocampus (rHp) produce robust deficits in a spatial Y-maze discrimination (YMD) test while sparing performance during contextual fear conditioning (CFC), comparable to results from lesions to homologous regions in mammals. In contrast, caudal hippocampus (cHp) lesions failed to produce deficits in either CFC or YMD, suggesting that, unlike mammals, both cHp and rHp of birds can support emotional behavior. These observations demonstrate functional segregation along the rostrocaudal axis of the avian Hp that is comparable in part to distinctions seen along the mammalian hippocampal septotemporal axis.

Protocol for inducing hippocampal formation lesions and associated behavioral testing in Japanese quail.

Here, we present a protocol for inducing selective lesions in the hippocampal formation of Japanese quail (Coturnix japonica), coupled with associated behavioral testing. We first describe the surgical procedure for aspiration lesions in Japanese quail. We then detail two well-known hippocampus-dependent behavioral tests adapted to birds-foraging array (FA) and spontaneous object recognition (SOR). This protocol is adapted from those used in mammals and can be used to study the involvement of Japanese quail memory centers in declarative memory. For complete details on the use and execution of this protocol, please refer to Damphousse et al. (2022).

Experience-Dependent Egr1 Expression in the Hippocampus of Japanese Quail.

The hippocampal formation (HF) is a structure critical to navigation and many forms of memory. In mammals, the firing of place cells is widely regarded as the fundamental unit of HF information processing. Supporting homology between the avian and mammalian HF, context-specific patterns of Egr1 have been reported in birds that are comparable to those produced by place cell firing in mammals. Recent electrophysiological data, however, suggest that many avian species lack place cells, potentially undermining the correspondence between Egr1 and place cell-related firing in the avian brain. To clarify this, the current study examines Egr1 expression in Japanese quail under conditions known to elicit only weakly spatially modulated firing patterns and report robust context-dependent Egr1 expression. These data confirm that context-dependent expression of Egr1 is not dependent on precise place fields and provide insight into how these birds are able to perform complex spatial tasks despite lacking mammalian-like place cells.

Dissociation of spatial and object memory in the hippocampal formation of Japanese quail.

The mammalian temporal cortex can be functionally segregated into regions that encode spatial information and others that are predominantly responsible for object recognition. In the present study, we report comparable functional segregation in the avian brain. Using Japanese quail, we find that bilateral lesions of the hippocampus (Hp) produce robust deficits in performance in a foraging array (FA) spatial memory task, while sparing spontaneous object recognition (SOR). In contrast, lesions to the adjacent area parahippocampalis (APH) compromise both SOR and FA. These observations demonstrate a functional dissociation between Hp and APH that is comparable to the distinctions seen in mammals between the hippocampus and surrounding temporal cortex.

Reaction to novelty as a behavioral assay of recognition memory in homing pigeons and Japanese quail.

Spontaneous novelty preference is apparent in a wide array of animals, including mammals, birds, reptiles, and fish. This provides a powerful behavioral assay to assess whether an animal can recognize a diverse array of stimuli in a common paradigm. Surprisingly, no research has been conducted in birds using novelty approach under conditions comparable to the spontaneous object recognition (SOR) protocols that have become standard across other animals. To correct this, the current study adapts a number of SOR protocols commonly used in mammals to characterize novelty approach in Silver King pigeons and Japanese quail. We show that, in general, both quail and pigeons readily approach novel objects or locations when tested using SOR protocols, although pigeons show a neophilic response under some conditions in which quail do not. Neither quail nor pigeons readily approach objects in novel contexts or novel locations. These data show that SOR can be successfully adapted to birds, allowing for more direct comparison between mammals and birds in tasks of shared ecological relevance.

Functional Integration of Adult-Generated Neurons in Diabetic Goto-Kakizaki Rats.

Adult-born neurons in the dentate gyrus (DG) make important contributions to learning as they integrate into neuronal networks. Neurogenesis is dramatically reduced by a number of conditions associated with cognitive impairment, including type 2 diabetes mellitus (T2DM). Increasing neurogenesis may thus provide a therapeutic target for ameliorating diabetes-associated cognitive impairments, but only if new neurons remain capable of normal function. To address the capacity for adult-generated neurons to incorporate into functional circuits in the hyperglycemic DG, we measured Egr1 expression in granule cells (GCs), BrdU labeled four weeks prior, in Goto-Kakizaki (GK) rats, an established model of T2DM, and age-matched Wistars. The results indicate that while fewer GCs are generated in the DG of GK rats, GCs that survive readily express Egr1 in response to spatial information. These data demonstrate that adult-generated GCs in the hyperglycemic DG remain functionally competent and support neurogenesis as a viable therapeutic target.

Experience-dependent persistent Arc expression is reduced in the aged hippocampus.

Aging is typically accompanied by both memory decline and changes in hippocampal function. Lasting memory is thought to also require recapitulation of recent memory traces during subsequent rest-a phenomenon termed memory trace reactivation or replay. Replay becomes less synchronized in the CA1 region of aged animals, and while subtle, this deficit may have profound physiological consequences for driving plasticity. Importantly, spike timing changes during replay may impair the induction of plasticity-regulating gene products, such as activity-regulated cytoskeletal protein (Arc). To test this hypothesis, Arc transcription was assessed both during spatial exploration and subsequent memory-related replay in hippocampal CA1 of young and aged animals. A significant age-related difference was observed in the pattern of pyramidal cells expressing Arc during rest, supporting the hypothesis that altered plasticity-related cascade is a major consequence of the changes in coordinated activity that occur during consolidation in older animals.

Pair foraging degrades socially transmitted food preferences in rats.

Following presentation of a novel food odor on the breath of a conspecific, naïve rats will exhibit a preference for that food, a form of learning called social transmission of food preference (STFP). When tested in isolation, STFPs are robust, persisting for up to a month and overcoming prior aversions. This testing protocol, however, does not account for rats' ecology. Rats and other rodents forage in small groups, rather than alone. We allowed rats to forage in pairs and found that, following social foraging, they no longer displayed a food preference, i.e., that STFPs degrade during social foraging. Non-foraging rats exposed to the same foods for the same amount of time in isolation maintained their preferences. We also examined whether individual differences between rats affect STFP. Neither boldness nor sociability predicted initial STFP strength, but bolder rats' preferences degraded more following social foraging. Shyer rats were more likely to eat at the same time as their partner. By tracking rats' interactions during social foraging, we show that they use complex rules to combine their own preferences with socially acquired information about foods in their environment. These results situate STFP within the behavioral ecology of foraging and suggest that individual traits and the interactions between them modulate how social learning is maintained, modified, or lost.

Attenuated Late-Phase Arc Transcription in the Dentate Gyrus of Mice Lacking Egr3.

The dentate gyrus (DG) engages in sustained Arc transcription for at least 8 hours following behavioral induction, and this time course may be functionally coupled to the unique role of the DG in hippocampus-dependent learning and memory. The factors that regulate long-term DG Arc expression, however, remain poorly understood. Animals lacking Egr3 show less Arc expression following convulsive stimulation, but the effect of Egr3 ablation on behaviorally induced Arc remains unknown. To address this, Egr3-/- and wild-type (WT) mice explored novel spatial environments and were sacrificed either immediately or after 5, 60, 240, or 480 minutes, and Arc expression was quantified by fluorescence in situ hybridization. Although short-term (i.e., within 60 min) Arc expression was equivalent across genotypes, DG Arc expression was selectively reduced at 240 and 480 minutes in mice lacking Egr3. These data demonstrate the involvement of Egr3 in regulating the late protein-dependent phase of Arc expression in the DG.