Research report
Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats

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Abstract

Environmental enrichment induces structural and biochemical changes in the brains of mammals that correlate with improved learning and memory. Research in rats suggests that social compared to inanimate stimulation might affect behavior differently, by acting upon dissociable neural substrates. Here we tested this hypothesis at the behavioral level by examining whether social and inanimate stimulation affect spatial memory formation and non-spatial discrimination reversal learning selectively. Spatial memory formation is known to depend on hippocampal–neocortical pathways, whereas reversal learning depends primarily on prefrontal cortico-striatal pathways. Male Lister hooded rats were housed singly or in groups of three in either small barren or large enriched cages, from weaning onwards. After 10 weeks of differential housing, spatial learning and memory were examined in the Morris water maze, followed by a series of tactile and odour discriminations, including discrimination reversal, in a two-choice discrimination task. Regardless of inanimate stimulation, social deprivation affected neither the acquisition of simple or complex discriminations, nor spatial memory formation, but was associated with impaired reversal learning in the two-choice discrimination task. By contrast, inanimate deprivation, regardless of social stimulation, affected neither acquisition nor reversal of two-choice discriminations, but selectively delayed the acquisition of spatial memory in the Morris water maze. This is the first demonstration of a double dissociation of early social and inanimate stimulation on two distinct behavioural functions that are mediated by dissociable underlying neural pathways. These findings strengthen the view that social and inanimate stimulation act, at least in part, upon dissociable neural substrates.

Introduction

In rats, environmental enrichment induces structural and biochemical changes in the brain that correlate with better learning and memory, and these effects are commonly attributed to the interaction of complex social and inanimate stimulation [49]. However, separate reviews on environmental enrichment [41], [49] and social isolation [17], [19], [43] suggest that social and inanimate stimulation affect behaviour differentially, and that they act, at least in part, upon dissociable underlying neural substrates. Furthermore, studies on social isolation and environmental enrichment have fundamentally different applications in biomedical research: environmental enrichment is used to model therapeutic effects on the course of neurodegenerative diseases (e.g. Huntington’s; [20]), ageing [22] and recovery from brain damage [21], while post-weaning social isolation is primarily used to model symptoms involved in schizophrenia (e.g. impaired pre-pulse inhibition; [15], [50]).

More specifically, while leaving simple forms of spatial or discrimination learning intact [24], [47], [53], isolation-rearing disrupts performance on tasks based on extinction learning [24], [32], [34], reversal learning [24] or the shifting of behavioural response rules [32], [33], [47], all of which require animals to inhibit previously reinforced responses. Deficits in the inhibitory control of behaviour have been attributed to impaired prefrontal cortico-striatal functioning [43]. In line with this, reversal learning is selectively impaired by lesions to areas within prefrontal cortex [5], [7], [27], [30] and striatum [12].

Conversely, rats raised in barren cages are primarily impaired in spatial learning and memory tasks that depend upon hippocampal–neocortical functioning [49], while being unimpaired in reversal learning [45], compared to rats raised in enriched environments. Indeed, lesion studies in rats have shown that spatial navigation in the water maze is selectively disrupted by hippocampal lesions [35], and enrichment-induced improvements in learning and memory correlate with neurogenesis in the hippocampus [25] and enhanced neural connectivity within hippocampus and neocortex [49].

Surprisingly, there is to date no study that tested by direct comparison whether social stimulation and inanimate stimulation have selective effects on these two structurally and functionally dissociable brain systems. Here we tested this hypothesis at the behavioural level. Rats were housed singly or in groups in either barren or enriched cages, from weaning onwards. As adults, spatial learning and memory were examined in the Morris water-maze, while non-spatial discrimination reversal learning was assessed in a two-choice discrimination task, to test whether social and inanimate stimulation have dissociable effects on spatial learning and reversal learning.

Section snippets

Animals and housing conditions

Subjects were 36 males derived from Lister hooded rats obtained from Harlan (Horst, The Netherlands), which were bred and raised at the ETH Research Unit Schwerzenbach (Switzerland). At weaning (postnatal day 21), from each of nine litters, four males were assigned one each to four housing treatments—“isolate in barren cage”, “isolate in enriched cage”, “group in barren cage”, “group in enriched cage”—according to a 2×2 factorial design with inanimate (barren (B) versus enriched (E) cage) and

Spatial learning

Barren housing significantly delayed the acquisition of spatial navigation, whereas social background had no effect on spatial learning (Fig. 1). Rats of the different treatment groups did not differ on the first day of training (path=14.21±0.85 m, mean±S.E.M.), and they all reached the same asymptotic level of performance near minimal path length towards the end of training (day 6: path=1.59±0.07 m). However, rats from enriched cages reached this level of performance within 3 days, whereas rats

Discussion

Social (single versus group housing) and inanimate stimulation (barren versus enriched cages) were varied independently in rats post-weaning to study the effects of early social and inanimate deprivation on spatial and reversal learning in adulthood. Social deprivation had no effect on the acquisition of tactile and odour discriminations in a two-choice discrimination task, and on spatial navigation in the Morris water maze, but selectively impaired reversal learning in the two-choice

Conclusions

The present results confirm and extend previous evidence suggesting dissociable effects of social and inanimate stimulation on cognitive functions that are mediated by dissociable neural pathways. Since the behavioural effects of either environmental factor (social or inanimate stimulation) are consistent across variation in the other, these results are likely to have high external validity [55]. They further highlight the importance of taking the animals’ environmental background into account

Acknowledgements

Many thanks go to Wolfgang Langhans for hosting the study and to the Animal Care Team of the Technical Services at the ETH laboratory in Schwerzenbach. This work was supported by Swiss Federal Veterinary Office Grants 002.4.2.97.8 (H.W.) and 002.4.2.98.4 (N.C.A.S.).

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