Social preference in rats not impacted by posterior parietal activity despite overall changes in familiarity-based social behavior

Recent literature points to a potential link between the evolution of complex social behavior and the posterior parietal cortex (PPC) in primates including humans (Parkinson & Wheatley, 2013). Thus far, this theory has been overlooked in other highly social animals that may have also evolved due to social selective pressures. In rodents, there is limited knowledge on the involvement of the PPC on sociality, and most studies of such behavior are limited to understanding social preference. We investigated the role of the PPC through two experiments using the 3-Chamber Sociability and Social Novelty test in rats (Crawley, 2004). In Experiment 1, we used a standard 3-Chamber paradigm, which included two novel demonstrators. In Experiment 2, this paradigm was altered to increase the difference in familiarity between demonstrators such that one demonstrator was highly familiar to the subject and the other was entirely novel. Rats with pre-testing permanent neurotoxic lesions were compared to sham surgery control rats, and the same rats were used for both experiments. Experiments 1 and 2 showed that both groups of rats preferred general social interaction, suggesting no deficit in sociability following PPC damage, regardless of demonstrator identity. Further, experimental and control rats showed similar levels of novelty preference following PPC damage, with novelty preferences increasing in Experiment 2. We argue that heightened novelty preference in Experiment 2 may reflect the increased difference in familiarity between demonstrators. Within the confines of the 3-Chamber task, our results suggest that PPC function was not required for general sociability or social novelty recognition. Because the PPC is implicated in abstract cognition, we argue that existing social tests in rodents may not adequately measure the complex cognitive capacities thought to be supported by the PPC. Future studies should investigate the role of the PPC in social cognition by employing behavioral tasks that require higher cognitive demand rather than testing inherent preference for social partners. Outside of our investigation of the PPC, these results show that social novelty preference can be manipulated through changes in familiarity of demonstrators, and that rats can discriminate others social identities.

Sex-dependent parameters of social behavior show marked variations between distinct laboratory mouse strains and their mixed offspring

Background: The survival of individuals of gregarious species depends on their ability to properly form social interactions. In humans, atypical social behavior is a hallmark of several psychopathological conditions, such as depression and autism spectrum disorder, many of which have sex-specific manifestations. Various strains of laboratory mice are used to reveal the mechanisms mediating typical and atypical social behavior in mammals. Methods: Here we used three social discrimination tests (social preference, social novelty preference, and sex preference) to characterize social behavior in males and females of three widely used laboratory mouse strains (C57BL/6J, BALB/c, and ICR). Results: We found marked sex- and strain-specific differences in the preference exhibited by subjects in a test-dependent manner. Interestingly, we found some characteristics that were strain-dependent, while others were sex-dependent. Moreover, even in the social preference test, where both sexes of all strains prefer social over object stimuli, we revealed sex- and strain-specific differences in the behavioral dynamics. We then cross-bred C57BL/6J and BALB/c mice and demonstrated that the offspring of such cross-breeding exhibit a profile of social behavior which is different from both parental strains and depends on the specific combination of parental strains. Conclusions: We conclude that social behavior of laboratory mice is highly sex- and strain-specific and strongly depends on genetic factors.

Oxytocin neurons mediates the effect of social isolation via the VTA circuits

Social interaction during adolescence strongly influences brain function and behaviour, and the recent pandemic has emphasized the devastating effect of social distancing on mental health. While accumulating evidences have shown the importance of the reward system in encoding specific aspects of social interaction, the consequences of social isolation on the reward system and the development of social skills later in adulthood are still largely unknown. Here, we found that one week of social isolation during adolescence in mice increased social interaction at the expense of social habituation and social novelty preference. Behavioural changes were accompanied by the acute hyperexcitability of dopamine (DA) neurons in the ventral segmental area (VTA) and long-lasting expression of GluA2-lacking AMPARs at excitatory inputs onto DA neurons that project to the prefrontal cortex (PFC). Social isolation-dependent behavioural deficits and changes in neural activity and synaptic plasticity were reversed by chemogenetic inhibition of oxytocin neurons in the paraventricular nucleus (PVN) of the hypothalamus. These results demonstrate that social isolation has acute and long-lasting effects on social interaction and suggest that these effects are mediated by homeostatic adaptations within the reward circuit.

Early environmental enrichment and impoverishment differentially affect addiction-related behavioral traits, cocaine-taking, and dopamine D2/3 receptor signaling in a rat model of vulnerability to drug abuse

Rationale Risk factors for drug addiction include genetics, environment, and behavioral traits such as impulsivity and novelty preference (NP), which have been related to deficits in striatal dopamine (DA) D2/3-receptors (D2/3R) and heightened amphetamine (AMPH)-induced DA release. However, the influence of the early rearing environment on these behavioral and neurochemical variables is not clear. Objectives We investigated the influence of early rearing environment on striatal D2/3R availabilities and AMPH-induced DA release in relation to impulsivity, NP, and propensity to drug self-administration (SA) in “addiction-prone” Roman high- (RHA) and “addiction-resistant” Roman low-avoidance (RLA) rats. Methods Animals were reared post-weaning in either environmental enrichment (EE) or impoverishment (EI) and were assessed at adulthood for impulsivity, NP, and propensity to cocaine SA. EE and EI rats were also scanned using single-photon emission computed tomography to concurrently measure in vivo striatal D2/3R availability and AMPH-induced DA release. Results EE vs. EI was associated with heightened impulsivity and a lack of NP in both rat lines. Higher dorsal striatal D2/3R densities were found in RHA EE and higher AMPH-induced DA release in RLA EE. Both impulsivity and NP were negatively correlated to dorsal striatal D2/3R availabilities and positively correlated with AMPH-induced DA release in EI but not in EE. EE vs. EI was related to a faster rate of cocaine intake and elevated active timeout responses in RHAs. Conclusion Our results suggest non-monotonic, environment-dependent, relationships between impulsivity, NP, and D2/3R-mediated signaling, and suggest that EI vs. EE may decrease the reinforcing effects of psychostimulants in predisposed individuals.

Young chicks rely on symmetry/asymmetry in perceptual grouping to discriminate sets of elements

Grouping sets of elements into smaller, equal-sized, subsets constitutes a perceptual strategy employed by humans and other animals to enhance cognitive performance. Here, we show that day-old chicks can solve extremely complex numerical discriminations (Exp.1), and that their performance can be enhanced by the presence of symmetrical/asymmetrical colour grouping (Exp.2 versus Exp.3). Newborn chicks were habituated for 1 h to even numerosities (sets of elements presented on a screen) and then tested for their spontaneous choice among what for humans would be considered a prime and a non-prime odd numerosity. Chicks discriminated and preferred the prime over the composite set of elements irrespective of its relative magnitude (i.e. 7 versus 9 and 11 versus 9). We discuss this result in terms of novelty preference. By employing a more complex contrast (i.e. 13 versus 15), we investigated the limits of such a mechanism and showed that induced grouping positively affects chicks' performance. Our results suggest the existence of a spontaneous mechanism that enables chicks to create symmetrical (i.e. same-sized) subgroups of sets of elements. Chicks preferentially inspected numerosities for which same-sized grouping is never possible (i.e. the prime numerosity) rather than numerosities allowing for symmetrical grouping (i.e. composite).

Developmental Trajectories of Picture-Based Object Representations during the First Year of Life

Experience with an object’s photo changes 9-month-olds’ preference for the referent object, confirming they can form picture-based object representations (Shinskey & Jachens, 2014). However, infants’ picture-based representations often appear weaker than object-based ones. The current study’s first objective was to investigate age differences in infants’ recognition memory for a real object after familiarization with its picture. The second objective was to test whether age differences in object permanence sensitivity with picture-based representations conceptually replicate those found with object-based representations, whereby 7-month-olds search more for familiar hidden objects but 11-month-olds search more for novel ones (Shinskey & Munakata, 2005; 2010). Twenty 6-month-olds and 20 11-month-olds were familiarized with an object’s photo and tested on their representation of the real referent object by comparing their preferential reaching for it versus a novel distractor object. The objects were visible in one condition testing recognition memory and hidden in another condition testing object permanence. Like 9-month-olds, 6- and 11-month-olds had a novelty preference with visible objects. This finding shows robust early recognition memory for an object after familiarization with its photo as well as developmental continuity. Unlike 9-month-olds, who switched to a familiarity preference with hidden objects, 6- and 11-month-olds switched to null preference. This U-shaped pattern fails to conceptually replicate 7- and 11-month-olds’ preferences with hidden objects after familiarization with a real object. It reveals discontinuity in sensitivity to an object’s permanence after familiarization with its picture, and suggests that such picture-based representations are weaker than object-based ones.

Long-term associative memory in rats: Effects of familiarization period in object-place-context recognition test

Spontaneous recognition tests, which utilize rodents’ innate tendency to explore novelty, can evaluate not only simple non-associative recognition memory but also more complex associative memory in animals. In the present study, we investigated whether the length of the object familiarization period (sample phase) improved subsequent novelty discrimination in the spontaneous object, place, and object-place-context (OPC) recognition tests in rats. In the OPC recognition test, rats showed a significant novelty preference only when the familiarization period was 30 min but not when it was 5 min or 15 min. In addition, repeated 30-min familiarization periods extended the significant novelty preference to 72 hours. However, the rats exhibited a successful discrimination between the stayed and replaced objects under 15 min and 30 min familiarization period conditions in the place recognition test and between the novel and familiar objects under all conditions of 5, 15 and 30 min in the object recognition test. Our results suggest that the extension of the familiarization period improves performance in the spontaneous recognition paradigms, and a longer familiarization period is necessary for long-term associative recognition memory than for non-associative memory.

Familiarity and Novelty in Aesthetic Preference: The Effects of the Properties of the Artwork and the Beholder

Familiarity and novelty are fundamental yet competing factors influencing aesthetic preference. However, whether people prefer familiar paintings or novel paintings has not been clear. Using both behavioral and eye-tracking measures, the present study aimed to investigate whether the effect of familiarity-novelty on aesthetic preference is independent or dependent on artwork properties (painting content, visual complexity) and viewer characteristics (experience in art). Participants were presented with two images of paintings, one of which was repeatedly presented but was always paired with a new painting in a randomized lateral arrangement. They were asked to indicate which of the two images they preferred with the degree of their preference. Behavioral results demonstrated an interactive influence of painting content and complexity on familiarity-novelty preference, especially alongside the distinction between representational and abstract paintings. Also, the familiarity-novelty preference was modulated by the degree of art experience, for abstract paintings in particular. Gaze results showed the differential effects of painting content, complexity, and art experience echoing the behavioral results. Taken together, the convergent results derived from behavioral and eye-tracking measures imply that novelty is an important feature of aesthetic appreciation, but its influence is modulated by properties of both the artwork and the beholder.

Curiosity Enhances Incidental Object Encoding in 8-month-old Infants

Recent research with adults indicates that curiosity induced by uncertainty enhances learning and memory outcomes, and that the resolution of curiosity has a special role in curiosity-driven learning. However, the role of curiosity-based learning in early development is unclear. Here we presented 8-month-old infants with a novel looking time procedure to explore: 1) whether uncertainty-induced curiosity enhances learning of incidental information; and 2) whether uncertainty-induced curiosity leads infants to seek uncertainty resolution over novelty. In Experiment 1, infants saw blurred images to induce curiosity (Curiosity sequence) or a clear image (Non-curiosity sequence) followed by presentation of incidental objects. Despite looking equally to the incidental objects in both sequences, in a subsequent object recognition phase infants looked longer to incidental objects presented in the Non-Curiosity than in the Curiosity condition, indicating that curiosity induced by blurred pictures enhanced processing of the incidental object, leading to a novelty preference for the incidental object in the Non-Curiosity condition. In Experiment 2, a blurred picture of a novel toy was first presented, followed by its corresponding clear picture paired with a clear picture of a new novel toy side-by-side. Infants showed no preference for either image, providing no evidence for a drive to resolve uncertainty. Overall, the current studies suggest that curiosity in infants has a broad attention-enhancing effect which contrasts with a more focused function of curiosity in adults..

Loss of Calretinin in L5a impairs the formation of the barrel cortex leading to abnormal whisker-mediated behaviors

The rodent whisker-barrel cortex system has been established as an ideal model for studying sensory information integration. The barrel cortex consists of barrel and septa columns that receive information input from the lemniscal and paralemniscal pathways, respectively. Layer 5a is involved in both barrel and septa circuits and play a key role in information integration. However, the role of layer 5a in the development of the barrel cortex remains unclear. Previously, we found that calretinin is dynamically expressed in layer 5a. In this study, we analyzed calretinin KO mice and found that the dendritic complexity and length of layer 5a pyramidal neurons were significantly decreased after calretinin ablation. The membrane excitability and excitatory synaptic transmission of layer 5a neurons were increased. Consequently, the organization of the barrels was impaired. Moreover, layer 4 spiny stellate cells were not able to properly gather, leading to abnormal formation of barrel walls as the ratio of barrel/septum size obviously decreased. Calretinin KO mice exhibited deficits in exploratory and whisker-associated tactile behaviors as well as social novelty preference. Our study expands our knowledge of layer 5a pyramidal neurons in the formation of barrel walls and deepens the understanding of the development of the whisker-barrel cortex system.